The Agriculturists 17(1&2): 66-75 (2019) ISSN 2304-7321 (Online), ISSN 1729-5211 (Print) A Scientific Journal of Krishi Foundation Indexed Journal

Morpho-physiological Response of Gliricidia sepium to Seawater-induced Salt Stress

M. A. Rahman1*, A. K. Das1, S. R. Saha1, M. M. Uddin2 and M. M. Rahman1

1Department of & Environment, and 2Department of Crop Botany Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur 1706, Bangladesh

*Corresponding author and Email: [email protected]

Received: 22 May 2019 Accepted: 09 November 2019

Abstract

Soil degradation due to the contamination of excessive saline water has been threatening health vis a vis plant productivity worldwide. Gliricidia sepium, a tree, has come into limelight in recent decades in Bangladesh due to its potency in improving . However, study on its suitability in coastal areas alongside identifying the salt-endurance limit is still lacking. Therefore, morpho- physiological attributes of G. sepium under seawater-induced different levels of salt stress were analyzed in a pot experiment from March to May 2018 to gain an insight into its salt-adaptive mechanisms. Results revealed that seawater-induced salinity negatively affected the growth-related attributes, such as plant height, fresh weight of shoots, dry weights of shoots and roots, and leaf area. The reduction of growth was coincided with reductions in photosynthetic pigments and relative water content. Interestingly, salt tolerance index was not decreased in parallel with increasing dosages of seawater, indicating the salt tolerance capacity of G. sepium. Furthermore, enhanced accumulation of proline increased the osmoprotective capacity of G. sepium in order to overcome the salt-induced osmotic stress. The results of the present study concluded that G. sepium might be suitable for growing in the salt prone areas ranging 20 – 40 dSm-1.

Keywords: Fertilizer tree, growth parameters, malondialdehyde, proline, photosynthetic pigments, soil salinity, salt tolerance index.

1. Introduction coastal ecosystems by degrading soil fertility, fresh water bodies and regeneration aptitude of Most of the parts of Bangladesh are more or less mangroves (Rahman et al., 2017). High salinity vulnerable to climatic menaces, but the coastal causes multifarious co-operative events that regions are predominantly very sensitive due to adversely affect plant growth and development, specific geo-climate and phylogenic activities. and consequently yields, resulting in reduction of Bangladesh has a coastal area of 2.85 million ha, agricultural outputs by billions of dollars per of which about 1.0 million ha along the coastal annum (Song and Wang, 2014; Tahjib-Ul-Arif et belt is under intimidation of different magnitudes al., 2018; Abdel Latef et al., 2019). Salt stress of salinities (Rahman et al., 2016). Furthermore, can trigger hyper-osmotic stress by reducing soil sea-level rise provokes the salinity intrusion in water availability and ion toxicity by the coastal plains causing demolition of the accumulating excessive Na+ in the cells, which 67 Response of Gliricidia sepium under salt stress severely impede common metabolic and content in the soil (Beedy et al., 2010; physiological functions, leading to plant death in Makumba, 2003; Kwesiga et al., 2003). severe cases (Rajput et al., 2016; Acosta-Motos Furthermore, it also improves the water et al., 2017). infiltration into the soil, increases water-holding capacity of the soil, reduces soil erosion, restores Apart from salinity problem, the organic matter and improves soil quality, and ultimately content in Bangladesh is less than 1%, increases the crop yields (Diouf et al., 2017). ranging between 0.05 and 0.9% in most cases, Growing Gliricidia plants on farm aile serves which also restraints the agricultural productivity dual purpose as they produce green leaf manure of Bangladesh (Biswas and Naher, 2019). that are rich in nitrogen (N) and helps in is intimately associated with food conserving soil through reduced soil erosion security and acts as a mainstay of Bangladesh’s (Rao et al., 2009). It is worth mentioning that economy, which employs nearly half of the total application of 1 t ha-1 Gliricidia leaf manure population and contributes 14.23% to the gross provides 21 kg N, 2.5 kg P, 18 kg K, 85 g Zn, domestic product (BER, 2019). The challenges 164 g Mn, 365 g Cu, 728 g Fe besides to sustainable land and/ or agricultural considerable quantities of S, Ca, Mg, B, Mo etc. management in Bangladesh are twofold. Firstly, (Srinivasarao et al., 2011). Farmers should to boost crop production and to maintain the soil therefore be encouraged to grow Gliricidia on a quality of the agricultural lands, secondly is to farm aile of fields for use in crop production, the improvement of degraded land in an which is a sustainable means of maintaining soil environmentally sustainable way (Karim et al., fertility along with reducing the pressure on 2014). In this context, adoption of climate-smart chemical that are environmentally organic agriculture, including crop residue perilous. recycling, legume plant inclusion in the cropping sequence or as intercrops, green leaf manuring Therefore, exploration of G. sepium towards and add-farmyard manure as supplementation or calamitous areas in Bangladesh will be one of alternation of chemical fertilizers will be a the auspicious options to serve the dual role, propitious option to improve the soil health and such as restoration of degraded soils and boost crop productivity (Srinivasarao et al., 2011). agricultural yield in an organic way. Unfortunately, being a new species in Gliricidia sepium (G. sepium), is a fast-growing Bangladesh (Hossain et al., 1996), salinity medium sized (10-15 m) leguminous tree tolerance limit alongside morpho-physiological belonging to the family Fabaceae. It is one of the response of G. sepium are not yet well best-known multipurpose trees originated from understood. Therefore, the present study was Central America and Mexico, but has also aimed to determine the salt tolerance limits as widely spread to West Africa, West Indies, well as appraise the effect of seawater induced Southern Asia and tropical America (Solangi et salt stress on the morpho-physiological features al., 2010). It adapts very well in a wide range of of G. sepium plants. soils ranging from eroded acidic (pH 4.5-6.2) soils, fertile sandy soils, heavy clay, calcareous 2. Materials and Methods limestone and alkaline soils (Wani et al., 2009). The tree is used for timber, firewood, hedges, 2.1. Study location, plant materials and growth medicinal purpose, charcoal, live fence, conditions plantation shade, poles, soil stabilization, and A pot experiment was conducted at the research even as mouse killer (Srinivasarao et al., 2011). field of the Department of Agroforestry and However, G. sepium has come into limelight in Environment, Bangabandhu Sheikh Mujibur recent decades to solve the soil fertility problem Rahman Agricultural University, Bangladesh due to its capacity of improving organic matter (24 09` N; 90 26` E) for a period of 3 months Rahman et al. /The Agriculturists 17(1&2): 66-75 (2019) 68

(March to May 2018). The study site is 8.2 m uniformly grown plants were irrigated with the above the sea level and characterized by a sub- diluted seawater (300 mL) every day for a period tropical climate with hot summer and mild of 90 days. The control plants were irrigated winter. The minimum and maximum with tap water. Root and shoot samples were temperatures of the research area were fluctuated harvested at 90th days of salt treatments for between 17 to 23C and 28 to 39C, determining various morpho-physiological and respectively, during the experimental period. biochemical parameters of G. sepium. Healthy G. sepium seeds were surface-sterilized in 5% (v/v) sodium hypochlorite solution 2.3. Determination of growth parameters containing 0.2% (v/v) Tween-20 for 30 min Plant height and leaf area were measured with a followed by five times washed with distilled linear scale and following the equation of water (dH2O). Subsequently, the surface- Carleton and Foote (1965), respectively. For sterilized seeds were incubated in dH2O at 26°C determining biomasses of shoots and roots, in the dark for 24 h. The seeds were then plants were carefully uprooted at day 90th of salt transferred to small polythene bags containing stress imposition and washed with distilled water 200 g of soils. Twenty-four days old G. sepium to remove adherent soil. Fresh weights (FWs) of seedlings of uniform size were transplanted into shoots, dry weights (DWs) of shoots and roots each pot (23 cm in height and 28 cm in were measured following the method described diameter). The pots were previously filled with by Mostofa et al., (2015). Salt tolerance index sandy loam soil mixture that was prepared by (STI) was calculated following the formula of mixing oven-dried soil and cow dung at the ratio Rahman et al. (2017). of 4:1 (in weight basis). However, the soils used was also treated with formaldehyde (2.5 mL 2.3. Determination of leaf relative water added in 100 mL of water) via spraying at the content, chlorophyll contents rate of 3.6-4.2 L of solution per m3 of soils to The fresh, turgid and dry weights of the leaves curtail the probability of developing soil-borne were used to determine leaf relative water diseases. Subsequently, mix thoroughly and kept content (RWC) according to the formula the soil covered for 24 h. After removing odor of described by Rahman et al., (2017). Chlorophyll formaldehyde, the soils were used to fill the pots. (Chl) and carotenoids (Car) contents of freshly In addition to cow dung, one liter of liquid collected leaf samples were determined using fertilizer containing 1% of-urea, triple super 80% acetone as previously described by Misratia phosphate and potassium sulphate was applied et al., (2013). once to each pot on 20 days old-transplanted seedlings. 2.4. Contents of proline The levels of proline (Pro) in shoots were 2.2. Treatments composition determined following the methods described by After transplanting the seedlings into pots, the Bates et al., (1973). plants were irrigated with tap water for 6 days for adaptation before being exposed to seawater- 2.5. Electrolyte leakage and lipid peroxidation induced salt stress. Seawater collected from Electrolyte leakage (EL) and the content of lipid southern coastal area (Cox’s Bazar sea beach) of peroxidation product [malondialdehyde (MDA)] Bangladesh (electrical conductivity of 69.6 dS m- in shoots were determined according to Lutts et 1, and Na+, K+, Ca2+ and Mg2+ concentrations of al., (1996) and Tayebimeigooni et al., (2012), 578.70, 20.38, 19.90 and 66.08 mmol L-1, respectively. respectively) was diluted with tap water to formulate different levels of salt treatments (20, 2.5. Statistical analysis 40 and 60 dS m-1) and the tap water was used as The data were subjected to a one-way analysis of control treatment. For imposing salt stress, the variance (ANOVA), following randomized block 69 Response of Gliricidia sepium under salt stress design and different letters indicate significant affected by salt stress. STI decreased by 46.87% differences among treatments at P<0.05, at the highest dosage of 60 dS m– 1 seawater and according to least significant difference test STI obtained 66.83 and 50.55% at 20 and 40 dS (LSD) using Statistix 10 package. Data presented m– 1, respectively (Table 1). Leaf area is the most are means ± standard errors (SEs) of three sensitive growth parameter in response to salt biological replications (n=3) for each treatment. stress (Qados, 2011). Reduction of leaf area progressively augmented with increasing salinity 3. Results and Discussion levels, and leaf area was found to reduce by 49.01, 51.49 and 57.55 % at day 90th in 3.1. Effects of salinity on plant height, FW of comparison to control upon application of 20, 40 shoots, DW of shoots and roots, STI and and 60 dS m-1 salinity levels to plants, leaf area of G. sepium respectively (Table 1). The attenuation of Salinity had considerable negative effects on growth-related parameters under high salinity plant height. This stress caused a significant clearly manifested that salt stress interferes reduction of plant height by 16.63, 25.94 and various physiological and metabolic processes of 35.26% at day 90th upon exposure of plants to 20, plant upon which growth relies on (Table 1). In 40 and 60 dS m-1 salinity levels, respectively, as general, plant growth is intricately connected to compared to the respective control values in G. meristem activity, cell division and expansion, sepium (Table 1). Similarly, shoot FWs was carbon fixation, as well as uptake of water and significantly attenuated by 46.74, 65.48 and nutrients (Pan et al., 2016; Rahman et al., 2016; 77.77% upon exposure of 90th day salt treatments Rahman et al., 2018). All of these processes are at the level of 20, 40 and 60 dS m-1 salinity rigorously affected by high salinity, resulting in levels, respectively, as compared to the reduced growth performance of plants, which is respective control values (Table 1). further supported by the findings of Rahman et Nevertheless, the negative consequences of al., (2018) in Achras sapota plant. However, the salinity on growth performance of G. sepium reduced leaf area observed in the salt-exposed were assessed by determining DW of shoots and plants (Table 1) might help in minimizing the roots. DW of salt-stressed shoots reduced by water loss by transpiration, which in turn can 30.72, 45.10 and 47.71%, whereas, root DW by favor the retention of toxic ions in the roots and 41.92, 65.38 and 73.08% at 20, 40 and 60 dS m-1 limiting the translocation of these ions to the salinity levels, respectively, compared to that of aerial parts of the plant (Theerawitaya et al., control. STI, a reliable criterion for salt tolerance 2015; Rangani et al., 2016; Rahman et al., (Abbas et al., 2013), was also differentially 2018).

Table 1. Effects of salinity on plant height, shoot fresh weight (FW), shoot and root-dry weight (DW), salt tolerance index (STI) and leaf area in G. sepium plants after 90 days exposure

Treatments Plant height Shoot FW Shoot DW Root DW STI Leaf area per (cm) (g) (g) (g) plant (cm2) Control 150.33±8.83a 103.13±1.45a 12.75±0.14a 3.47±0.35a - 1618.72±20.49a 20dS/m 125.33±3.76b 54.93±1.98b 8.83±0.30b 2.01±0.01b 66.87+1.88a 825.40±21.86b 40dS/m 111.33±2.03bc 35.6±1.41c 7.00±0.14c 1.20±0.23bc 50.57+0.53b 785.20±30.24b 60dS/m 97.33±4.06c 22.93±1.97d 6.67±0.44c 0.93±0.13c 46.87+2.68b 687.20±11.02c

Values are means ± standard errors of three biological replications (n = 3). Different superscripted letters within a column indicate statistically significant differences among the treatments according to a least significant difference test (P < 0.05). FW, fresh weight; DW, dry weight; STI, salt tolerance index. Rahman et al. /The Agriculturists 17(1&2): 66-75 (2019) 70

Figure 1. Effects of salinity (0, 20, 40 and 60 dS m−1) on (a) Chl a, (b) Chl b, (c) Chl (a+b) (d) Car content of Gliricidia sepium after 90 days exposure. Bars represent standard errors of the means (n = 3). Different letters indicate significant differences among the treatments at P < 0.05, according to a least significant difference test. Chl, Chlorophyll; Car, Carotenoid; FW, fresh weight.

71 Response of Gliricidia sepium under salt stress

Figure 2. Effects of salinity on (a) relative water content, (b) proline, (c) electrolyte leakage (d) malondialdehyde (MDA) content of Gliricidia sepium after 90 days exposure (0, 20, 40 and 60 dS m−1). Bars represent standard errors of the means (n = 3). Different letters indicate significant differences among the treatments at P < 0.05, according to a least significant difference test. FW, fresh weight.

Rahman et al. /The Agriculturists 17(1&2): 66-75 (2019) 72

3.2. Effects of salinity on photosynthetic 3.3. Effects of salinity on leaf RWC, content of pigment Pro, leaf EL, and MDA of G. sepium In response to seawater-induced salinity, leaf Irrigation of G. sepium plants with diluted RWC decreased by 10.10, 21.98 and 31.16% at seawater caused gradual and significant day 90th under 20, 40 and 60 dS m-1 salinity decreases in the contents of Chl a (by 4.35, 10.06 levels, respectively, compared to control (Fig. and 28.26% at day 90th), Chl b (by 5.86, 16.50 2a). To understand the mechanisms associated and 44.15% at day 90th), total Chls (by 5.21, with osmotic adjustment under salt stress, we 12.39 and 33.75% at day 90th) and carotenoid have determined the level of Pro in G. sepium content (by 14.52, 25.19 and 36.64% at day 90th) plants under normal and salt stress conditions. upon imposition of 20, 40 and 60 dS m-1 salinity, Pro content remarkably increased by 161.99, respectively, compared with plants irrigated with 201.95 and 214.91 % at day 90th upon imposition tap water (Fig. 1). Photosynthetic efficiency of a of 20, 40 and 60 dS m-1 diluted seawater, plant determines the overall performance, which respectively, compared to control (Fig. 2b). To is emulated by growth and biomass parameters. assess the cell membrane integrity under salt In the current study, the levels of Chl a and b, as stress, we determined the level of EL in the well as total Chls, were progressively declined shoots of G. sepium (Fig. 2c). At day 90th of salt with the rise of salinity level and exposure time, imposition, EL content significantly increased by indicating that the photosynthetic performance of 361.43 and 495.96% at 20 and 40 dS m-1 salinity G. sepium was hampered, which contributed to levels, respectively, relative to control. the decrease in plant biomass (Fig. 1; Table 1). Nevertheless, the increment of EL levels showed the maximum 823.73% at the highest salinity The reduction in Chl levels and consequent dose (60 dS m-1) than that of untreated respective biomass loss were evident in other studies under control. To assess the cell membrane integrity salt stress, and the possible cause was attributed under salt stress, we determined the levels of to the direct effects of accumulated Na+ and ROS lipid peroxidation product MDA in the shoots of (Qin et al., 2010; Mostofa et al., 2015). Chl a is G. sepium MDA content significantly increased the most abundant and integral part of the light- by 22.83, 34.82 and 97.50% at day 90th upon harvesting complex, whereas Chl b as an imposition of 20, 40 and 60 dS m-1 salinity, accessory pigment acts indirectly in respectively, compared to control plants (Fig. photosynthesis by transmitting photons to the 2d). In the present study, reduction of leaf RWC Chl a (Chen, 2014; Gururani et al., 2015). Thus, in salt-stressed plants upon exposure to salinity a higher level of Chl a than Chl b at all indicating the salt-mediated induction of concentrations of seawater (Fig. 1a, b) might physiological water deficit in G. sepium (Fig. have contributed to the improved efficiency of 2a). However, enhanced accumulation of Pro in G. sepium in resisting salt-induced loss of salt-stressed plants might help adjust to water photosynthetic capacity (Table 1), as was deficit conditions (Fig. 2b). Pro is known to reported in Atriplex helimus by Bendaly et al., provide improved protection against salinity by (2016) and in Acacia auriculiformis plant by scavenging free radicals, stabilizing membranes, Rahman et al., (2017). Besides functioning as proteins and enzymes, and maintaining ion accessory pigments, carotenoids are known to be homeostasis (Kishor and Sreenivasulu, 2014). involved in protecting photosynthetic reaction Nonetheless, higher accumulation of toxic ions center from chlorophyll-mediated generation of under salt stress lead to the generation of reactive 1 singlet oxygen ( O2) by quenching triplet states oxygen species (ROS). ROS predominantly of Chls, and thus stabilizing and protecting the attacks the membrane, causing lipid peroxidation lipid phase of thylakoid membrane (Gururani et that leads to the generation of MDA and loss of al., 2015). essential electrolytes (Penella et al., 2016). The levels of MDA content and EL in G. sepium 73 Response of Gliricidia sepium under salt stress plants enhanced to a lower extent at low and Abdel Latef, AAH., Mostofa MG., Rahman moderate salinity levels (20-40 dS m-1), where it MM., Abdel-Farid IB., Tran LSP. 2019. was sharply increased at high dosage of salinity Extracts from yeast and carrot roots (60 dS m-1), which indicate that G. sepium plants enhance maize performance under could resist themselves from salt-induced seawater-induced salt stress by altering membrane damage up to a certain level of physio-biochemical characteristics of salinity. stressed plants. Journal of Plant Growth Regulation, 1–14. 4. Conclusions Acosta-Motos JR., Ortuño MF., Bernal-Vicente

A., Diaz-Vivancos P., Sanchez-Blanco Our findings concluded that exposure of G. MJ., Hernandez JA. 2017. Plant responses sepium plants to seawater-induced salinity to salt stress: adaptive mechanisms. adversely affects the performance of the whole Agronomy, 7: 18. plant, particularly by inhibiting growth and development. Nevertheless, the adapted stress Bates LS., Waldren RP., Teare ID. 1973. Rapid tolerance mechanisms of G. sepium at a salinity determination of free proline for water- range of 20 – 40 dsm-1 could be attributed to (1) stress studies. Plant and Soil, 39(1):205- maintained higher dry biomass, (2) maintained 207. optimum water status in terms of elevated RWC, (3) abundance of primary photosynthetic Beedy TL., Snapp SS., Akinnifesi FK., Sileshi GW. 2010. Impact of Gliricidia sepium pigment Chl a over accessory pigment Chl b to intercropping on soil organic matter sustain favourable photosynthetic rate, and (4) fractions in a maize-based cropping accumulation of osmolyte like Pro to maintain system. Agriculture, Ecosystems and osmoprotectant capacity under salt-stress. Environment, 138(3-4):139-146. Nevertheless, we postulated that established plants of this species might be tolerant to salt Bendaly A., Messedi D., Smaoui A., Ksouri R., stress higher than the level used in this study Bouchereau A., Abdelly C. 2016. because seedlings are more sensitive to high Physiological and leaf metabolome soluble salt levels than established plants. changes in the xerohalophyte species Atriplex halimus induced by 5. Acknowledgements salinity. Plant Physiology and Biochemistry, 103:208-218. This study was funded by National Science and Technology (NST). We also thank all faculty Bangladesh Economic Review (BER). 2019. members and staffs of Department of Ministry of Finance, Government of Agroforestry and Environment, Bangabandhu Bagladesh. Sheikh Mujibur Rahman Agricultural University, Biswas JC., Naher UA. 2019. Soil nutrient stress Bangladesh. All authors read and approved the and rice production in Bangladesh. In final manuscript. Advances in Rice Research for Abiotic Stress Tolerance, Woodhead Publishing, References 431-445 pp.

Carleton AE., Foote WH. 1965. A comparison of Abbas MK., Ali AS., Hasan HH., Ghal RH. methods for estimating total leaf area of 2013. Salt tolerance study of six cultivars barley plants 1. Crop Science, 5(6):602- of rice (Oryza sativa L.) during 603. germination and early seedling growth. Journal of Agricultural Science, 5:250- Chen M. 2014. Chlorophyll modifications and 259. their spectral extension in oxygenic Rahman et al. /The Agriculturists 17(1&2): 66-75 (2019) 74

photosynthesis. Annual Review of Malawi. PhD Thesis, Wagenigen Biochemistry, 83:317-340. University and Research Centre, Wagenigen, The Netherlands. Diouf A., Ndiaye M., Fall-Ndiaye MA., Diop TA. 2017. Maize crop N uptake from Misratia KM., Ismail MR., Hakim MA., Musa organic material of Gliricidia sepium MH., Puteh A. 2013. Effect of salinity and coinoculated with rhizobium and alleviating role of gibberellic acid (GA3) Arbuscular mycorrhizal fungus in Sub- for improving the morphological, Saharian Africa sandy soil. American physiological and yield traits of rice Journal of Plant Sciences, 8(3):428. varieties. Australian Journal of Crop Science, 7(11):1682. Gururani MA., Venkatesh J., Tran LSP. 2015. Regulation of photosynthesis during Mostofa MG., Saegusa D., Fujita M., Tran LSP. abiotic stress-induced photoinhibition. 2015. Hydrogen sulfide regulates salt Molecular Plant, 8(9):1304-1320. tolerance in rice by maintaining Na+/K+ balance, mineral homeostasis and Hossain MK., Islam SA., Islam QN., Tarafdar oxidative metabolism under excessive salt MA., Zashimuddin M. 1996. Growth and stress. Frontiers in Plant Science, 6:1055. biomass productions of the international provenance trial of Gliricidia sepium in Pan YQ., Guo H., Wang SM., Zhao B., Zhang Bangladesh. Chittagong University JL., Ma Q., Yin HJ., Bao AK. 2016. The Studies, Science, 20(1):77-82. photosynthesis, Na+/K+ homeostasis and osmotic adjustment of Atriplex canescens Karim Z., Qureshi BA., Mumtaz M., Qureshi S. in response to salinity. Frontiers in Plant 2014. Heavy metal content in urban soils Science, 7:848. as an indicator of anthropogenic and natural influences on landscape of Penella C., Landi M., Guidi L., Nebauer SG., Karachi-a multivariate spatio-temporal Pellegrini E., San Bautista A., Remorini analysis. Ecological Indicators, 42:20-31. D., Nali C., López-Galarza S., Calatayud A. 2016. Salt-tolerant rootstock increases Kishor PBK., Sreenivasulu N. 2014. Is proline yield of pepper under salinity through accumulation per se correlated with stress maintenance of photosynthetic tolerance or is proline homeostasis a more performance and sinks strength. Journal critical issue?. Plant, Cell and of Plant Physiology, 193:1-11. Environment, 37(2):300-311. Qados AMA. 2011. Effect of salt stress on plant Kwesiga F., Akinnifesi FK., Mafongoya PL., McDermott MH., Agumya A. 2003. growth and metabolism of bean plant Agroforestry research and development in Vicia faba (L.). Journal of the Saudi southern Africa during the 1990s: review Society of Agricultural Sciences, 10(1):7- and challenges ahead. Agroforestry 15. Systems, 59(3):173-186. Qin J., Dong WY., He KN., Yu Y., Tan GD., Lutts S., Kinet JM., Bouharmont J. 1996. NaCl- Han L., Dong M., Zhang YY., Zhang D., induced senescence in leaves of rice Li AZ., Wang ZL. 2010. NaCl salinity- (Oryza sativa L.) cultivars differing in salinity resistance. Annals of induced changes in water status, ion Botany, 78(3):389-398. contents and photosynthetic properties of Shepherdia argentea (Pursh) Nutt. Makumba W. 2003. Nitrogen use efficiency and carbon sequestration in legume tree-based seedlings. Plant, Soil and agroforestry systems. A case study in Environment, 56(7):325-332. 75 Response of Gliricidia sepium under salt stress

Rahman MM., Haque MA., Nihad SAI., coconut plantations of Pakistan. Pakistan Howlader MRA., Akand MMH. 2016. Journal of Botany, 42(2):825-832. Morpho-physiological response of Acacia Song J., Wang B. 2014. Using euhalophytes to auriculiformis as influenced by seawater understand salt tolerance and to develop induced salinity stress. Forest Systems, saline agriculture: Suaeda salsa as a 25(3):071. promising model. Annals of Rahman MM., Mostofa MG., Rahman MA., Botany, 115(3):541-553. Miah MG., Saha SR., Karim MA., Tran Srinivasarao C., Venkateswarlu B., Dinesh Babu LSP. 2018. Insight into salt tolerance M., Wani SP., Dixit S., Sahrawat KL., mechanisms of the halophyte Achras Sumanta K. 2011. Soil health sapota: an important fruit tree for improvement with Gliricidia green leaf agriculture in coastal areas. Protoplasma, manuring in rainfed agriculture, on farm 256(1):181-191. experiences. Central Research Institute for doi.org/10.1007/s00709-018-1289-y. Dryland Agriculture, Santoshnagar, PO Rahman MM., Rahman MA., Miah MG., Saha Saidabad, Hyderabad. SR., Karim MA., Mostofa MG. 2017. Tahjib-Ul-Arif M., Siddiqui MN., Sohag AAM., Mechanistic Insight into salt tolerance of Sakil MA., Rahman MM., Polash MAS., Acacia auriculiformis: the importance of Mostofa MG., Tran LSP. 2018. Salicylic ion selectivity, osmoprotection, tissue acid-mediated enhancement of tolerance, and Na+ exclusion. Frontiers in photosynthesis attributes and antioxidant Plant Science, 8:155. capacity contributes to yield improvement Rajput VD., Minkina T., Yaning C., Sushkova of maize plants under salt stress. Journal S., Chapligin VA., Mandzhieva S. 2016. of Plant Growth Regulation, 37(4):1318- A review on salinity adaptation 1330. mechanism and characteristics of Populus Tayebimeigooni A., Awang Y., Mahmood M., euphratica, a boon for arid Selamat A., Wahab Z. 2012. Leaf water ecosystems. Acta Ecológica status, proline content, lipid peroxidation Sinica, 36(6):497-503. and accumulation of hydrogen peroxide in Rangani J., Parida AK., Panda A., Kumari A. salinized Chinese kale (Brassica 2016. Coordinated changes in alboglabra). Journal of Food, Agriculture antioxidative enzymes protect the and Environment, 10:371-374. photosynthetic machinery from salinity Theerawitaya C., Tisarum R., Samphumphuang induced oxidative damage and confer salt tolerance in an extreme halophyte T., Singh HP., Cha-Um S., Kirdmanee C., Salvadora persica L. Frontiers in Plant Takabe T. 2015. Physio-biochemical and Science, 7: 50. morphological characters of halophyte Rao CS., Wani SP., Sahrawat KL., Rajasekharao legume shrub, Acacia ampliceps seedlings B. 2009. strategies in response to salt stress under in participatory watersheds in semi-arid greenhouse. Frontiers in Plant tropical India. Indian Journal of Science, 6:630. Fertilisers, 5(12):113-128. Wani SP., Rockström J., Oweis TY. 2009. Solangi AH., Mal B., Kazmi AR., Iqbal MZ. Rainfed agriculture: unlocking the 2010. Preliminary studies on the major potential, eds., (Vol. 7), Centre for characteristic, agronomic feature and nutrient value of Gliricidia sepium in Agriculture and Bioscience International.